Skip to main content
NCBI home page
Journal of Virology logoLink to Journal of Virology
. 1995 Feb;69(2):1085–1092. doi: 10.1128/jvi.69.2.1085-1092.1995

Rhinovirus-mediated endosomal release of transfection complexes.

W Zauner 1, D Blaas 1, E Kuechler 1, E Wagner 1
PMCID: PMC188680  PMID: 7815487

Abstract

Endocytosis is an efficient method for transfer of genes into mammalian cells. Incorporation of adenovirus particles into gene transfer complexes greatly enhances gene delivery, probably by the release of endocytosed DNA into the cytoplasm. We report here that two different serotypes of human rhinovirus (HRV), HRV2 and HRV14, are also able to enhance receptor-mediated gene transfer. The effect of several compounds known to inhibit viral infection on HRV2- and HRV14-enhanced transfection was examined. WIN I(s) and WIN IV, two compounds which inhibit viral uncoating, had different effects on HRV2- and HRV14-enhanced gene transfer to NIH 3T3 cells. While HRV14-enhanced gene transfer was severely reduced in the presence of these compounds, virtually no effects were observed when HRV2 was used. The use of antiviral compounds thus allowed transfection of human cells, which are normally lysed rapidly upon infection with HRV. Viral activity could be mimicked by using a peptide derived from the N terminus of VP1 of HRV2. This peptide possesses pH-dependent membrane-disrupting activity and enhances gene transfer to NIH 3T3 and HeLa cells.

Full Text

The Full Text of this article is available as a PDF (482.0 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Badger J., Minor I., Kremer M. J., Oliveira M. A., Smith T. J., Griffith J. P., Guerin D. M., Krishnaswamy S., Luo M., Rossmann M. G. Structural analysis of a series of antiviral agents complexed with human rhinovirus 14. Proc Natl Acad Sci U S A. 1988 May;85(10):3304–3308. doi: 10.1073/pnas.85.10.3304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Colonno R. J., Callahan P. L., Long W. J. Isolation of a monoclonal antibody that blocks attachment of the major group of human rhinoviruses. J Virol. 1986 Jan;57(1):7–12. doi: 10.1128/jvi.57.1.7-12.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cotten M., Wagner E., Birnstiel M. L. Receptor-mediated transport of DNA into eukaryotic cells. Methods Enzymol. 1993;217:618–644. doi: 10.1016/0076-6879(93)17092-j. [DOI] [PubMed] [Google Scholar]
  4. Cotten M., Wagner E., Zatloukal K., Birnstiel M. L. Chicken adenovirus (CELO virus) particles augment receptor-mediated DNA delivery to mammalian cells and yield exceptional levels of stable transformants. J Virol. 1993 Jul;67(7):3777–3785. doi: 10.1128/jvi.67.7.3777-3785.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Curiel D. T., Agarwal S., Wagner E., Cotten M. Adenovirus enhancement of transferrin-polylysine-mediated gene delivery. Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8850–8854. doi: 10.1073/pnas.88.19.8850. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. ELLMAN G. L. Tissue sulfhydryl groups. Arch Biochem Biophys. 1959 May;82(1):70–77. doi: 10.1016/0003-9861(59)90090-6. [DOI] [PubMed] [Google Scholar]
  7. Fox M. P., Otto M. J., McKinlay M. A. Prevention of rhinovirus and poliovirus uncoating by WIN 51711, a new antiviral drug. Antimicrob Agents Chemother. 1986 Jul;30(1):110–116. doi: 10.1128/aac.30.1.110. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fricks C. E., Hogle J. M. Cell-induced conformational change in poliovirus: externalization of the amino terminus of VP1 is responsible for liposome binding. J Virol. 1990 May;64(5):1934–1945. doi: 10.1128/jvi.64.5.1934-1945.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gao L., Wagner E., Cotten M., Agarwal S., Harris C., Rømer M., Miller L., Hu P. C., Curiel D. Direct in vivo gene transfer to airway epithelium employing adenovirus-polylysine-DNA complexes. Hum Gene Ther. 1993 Feb;4(1):17–24. doi: 10.1089/hum.1993.4.1-17. [DOI] [PubMed] [Google Scholar]
  10. Greber U. F., Willetts M., Webster P., Helenius A. Stepwise dismantling of adenovirus 2 during entry into cells. Cell. 1993 Nov 5;75(3):477–486. doi: 10.1016/0092-8674(93)90382-z. [DOI] [PubMed] [Google Scholar]
  11. Greve J. M., Davis G., Meyer A. M., Forte C. P., Yost S. C., Marlor C. W., Kamarck M. E., McClelland A. The major human rhinovirus receptor is ICAM-1. Cell. 1989 Mar 10;56(5):839–847. doi: 10.1016/0092-8674(89)90688-0. [DOI] [PubMed] [Google Scholar]
  12. Greve J. M., Forte C. P., Marlor C. W., Meyer A. M., Hoover-Litty H., Wunderlich D., McClelland A. Mechanisms of receptor-mediated rhinovirus neutralization defined by two soluble forms of ICAM-1. J Virol. 1991 Nov;65(11):6015–6023. doi: 10.1128/jvi.65.11.6015-6023.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hofer F., Gruenberger M., Kowalski H., Machat H., Huettinger M., Kuechler E., Blaas D. Members of the low density lipoprotein receptor family mediate cell entry of a minor-group common cold virus. Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1839–1842. doi: 10.1073/pnas.91.5.1839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hoover-Litty H., Greve J. M. Formation of rhinovirus-soluble ICAM-1 complexes and conformational changes in the virion. J Virol. 1993 Jan;67(1):390–397. doi: 10.1128/jvi.67.1.390-397.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hughes J. H., Thomas D. C., Hamparian V. V., Cramblett H. G. Acid liability of rhinovirus type 14: effect of pH, time, and temperature. Proc Soc Exp Biol Med. 1973 Nov;144(2):555–560. doi: 10.3181/00379727-144-37634. [DOI] [PubMed] [Google Scholar]
  16. Lim K., Chae C. B. A simple assay for DNA transfection by incubation of the cells in culture dishes with substrates for beta-galactosidase. Biotechniques. 1989 Jun;7(6):576–579. [PubMed] [Google Scholar]
  17. MacDonald R. C., MacDonald R. I., Menco B. P., Takeshita K., Subbarao N. K., Hu L. R. Small-volume extrusion apparatus for preparation of large, unilamellar vesicles. Biochim Biophys Acta. 1991 Jan 30;1061(2):297–303. doi: 10.1016/0005-2736(91)90295-j. [DOI] [PubMed] [Google Scholar]
  18. MacGregor G. R., Caskey C. T. Construction of plasmids that express E. coli beta-galactosidase in mammalian cells. Nucleic Acids Res. 1989 Mar 25;17(6):2365–2365. doi: 10.1093/nar/17.6.2365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Madshus I. H., Olsnes S., Sandvig K. Different pH requirements for entry of the two picornaviruses, human rhinovirus 2 and murine encephalomyocarditis virus. Virology. 1984 Dec;139(2):346–357. doi: 10.1016/0042-6822(84)90380-5. [DOI] [PubMed] [Google Scholar]
  20. Maynell L. A., Kirkegaard K., Klymkowsky M. W. Inhibition of poliovirus RNA synthesis by brefeldin A. J Virol. 1992 Apr;66(4):1985–1994. doi: 10.1128/jvi.66.4.1985-1994.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. McKinlay M. A., Pevear D. C., Rossmann M. G. Treatment of the picornavirus common cold by inhibitors of viral uncoating and attachment. Annu Rev Microbiol. 1992;46:635–654. doi: 10.1146/annurev.mi.46.100192.003223. [DOI] [PubMed] [Google Scholar]
  22. Neubauer C., Frasel L., Kuechler E., Blaas D. Mechanism of entry of human rhinovirus 2 into HeLa cells. Virology. 1987 May;158(1):255–258. doi: 10.1016/0042-6822(87)90264-9. [DOI] [PubMed] [Google Scholar]
  23. Ohkuma S., Poole B. Cytoplasmic vacuolation of mouse peritoneal macrophages and the uptake into lysosomes of weakly basic substances. J Cell Biol. 1981 Sep;90(3):656–664. doi: 10.1083/jcb.90.3.656. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Pevear D. C., Fancher M. J., Felock P. J., Rossmann M. G., Miller M. S., Diana G., Treasurywala A. M., McKinlay M. A., Dutko F. J. Conformational change in the floor of the human rhinovirus canyon blocks adsorption to HeLa cell receptors. J Virol. 1989 May;63(5):2002–2007. doi: 10.1128/jvi.63.5.2002-2007.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Plank C., Zatloukal K., Cotten M., Mechtler K., Wagner E. Gene transfer into hepatocytes using asialoglycoprotein receptor mediated endocytosis of DNA complexed with an artificial tetra-antennary galactose ligand. Bioconjug Chem. 1992 Nov-Dec;3(6):533–539. doi: 10.1021/bc00018a012. [DOI] [PubMed] [Google Scholar]
  26. Seglen P. O. Inhibitors of lysosomal function. Methods Enzymol. 1983;96:737–764. doi: 10.1016/s0076-6879(83)96063-9. [DOI] [PubMed] [Google Scholar]
  27. Skern T., Sommergruber W., Blaas D., Pieler C., Kuechler E. Relationship of human rhinovirus strain 2 and poliovirus as indicated by comparison of the polymerase gene regions. Virology. 1984 Jul 15;136(1):125–132. doi: 10.1016/0042-6822(84)90253-8. [DOI] [PubMed] [Google Scholar]
  28. Szoka F., Jr, Papahadjopoulos D. Procedure for preparation of liposomes with large internal aqueous space and high capture by reverse-phase evaporation. Proc Natl Acad Sci U S A. 1978 Sep;75(9):4194–4198. doi: 10.1073/pnas.75.9.4194. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Wagner E., Cotten M., Mechtler K., Kirlappos H., Birnstiel M. L. DNA-binding transferrin conjugates as functional gene-delivery agents: synthesis by linkage of polylysine or ethidium homodimer to the transferrin carbohydrate moiety. Bioconjug Chem. 1991 Jul-Aug;2(4):226–231. doi: 10.1021/bc00010a006. [DOI] [PubMed] [Google Scholar]
  30. Wagner E., Plank C., Zatloukal K., Cotten M., Birnstiel M. L. Influenza virus hemagglutinin HA-2 N-terminal fusogenic peptides augment gene transfer by transferrin-polylysine-DNA complexes: toward a synthetic virus-like gene-transfer vehicle. Proc Natl Acad Sci U S A. 1992 Sep 1;89(17):7934–7938. doi: 10.1073/pnas.89.17.7934. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Wagner E., Zatloukal K., Cotten M., Kirlappos H., Mechtler K., Curiel D. T., Birnstiel M. L. Coupling of adenovirus to transferrin-polylysine/DNA complexes greatly enhances receptor-mediated gene delivery and expression of transfected genes. Proc Natl Acad Sci U S A. 1992 Jul 1;89(13):6099–6103. doi: 10.1073/pnas.89.13.6099. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Wilcox D. K., Kitson R. P., Widnell C. C. Inhibition of pinocytosis in rat embryo fibroblasts treated with monensin. J Cell Biol. 1982 Mar;92(3):859–864. doi: 10.1083/jcb.92.3.859. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Yin F. H., Lomax N. B. Host range mutants of human rhinovirus in which nonstructural proteins are altered. J Virol. 1983 Nov;48(2):410–418. doi: 10.1128/jvi.48.2.410-418.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Yoshimura K., Rosenfeld M. A., Seth P., Crystal R. G. Adenovirus-mediated augmentation of cell transfection with unmodified plasmid vectors. J Biol Chem. 1993 Feb 5;268(4):2300–2303. [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES